Spontaneous mutations in maize pollen are frequent in some lines and arise mainly from retrotranspositions and deletions

Hugo K. Dooner, Qinghua Wang, Jun T. Huang, Yubin Li, Limei He, Wenwei Xiong, Chunguang Du

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

While studying spontaneous mutations at the maize bronze (bz) locus, we made the unexpected discovery that specific low-copy number retrotransposons are mobile in the pollen of some maize lines, but not of others. We conducted large-scale genetic experiments to isolate new bz mutations from several Bz stocks and recovered spontaneous stable mutations only in the pollen parent in reciprocal crosses. Most of the new stable bz mutations resulted from either insertions of low-copy number long terminal repeat (LTR) retrotransposons or deletions, the same two classes of mutations that predominated in a collection of spontaneous wx mutations [Wessler S (1997) The Mutants of Maize, pp 385–386]. Similar mutations were recovered at the closely linked sh locus. These events occurred with a frequency of 2–4 × 10−5 in two lines derived from W22 and in 4Co63, but not at all in B73 or Mo17, two inbreds widely represented in Corn Belt hybrids. Surprisingly, the mutagenic LTR retrotransposons differed in the active lines, suggesting differences in the autonomous element make-up of the lines studied. Some active retrotransposons, like Hopscotch, Magellan, and Bs2, a Bs1 variant, were described previously; others, like Foto and Focou in 4Co63, were not. By high-throughput sequencing of retrotransposon junctions, we established that retrotranposition of Hopscotch, Magellan, and Bs2 occurs genome-wide in the pollen of active lines, but not in the female germline or in somatic tissues. We discuss here the implications of these results, which shed light on the source, frequency, and nature of spontaneous mutations in maize.

Original languageEnglish
Pages (from-to)10734-10743
Number of pages10
JournalProceedings of the National Academy of Sciences of the United States of America
Volume166
Issue number22
DOIs
StatePublished - 28 May 2019

Fingerprint

Pollen
Zea mays
Retroelements
Mutation
Terminal Repeat Sequences
Genome

Keywords

  • Inbred variation
  • LTR retrotransposon
  • Maize
  • Male sporogenesis
  • Spontaneous mutation

Cite this

@article{1910c37ab8a6443c9cb4690f668abda2,
title = "Spontaneous mutations in maize pollen are frequent in some lines and arise mainly from retrotranspositions and deletions",
abstract = "While studying spontaneous mutations at the maize bronze (bz) locus, we made the unexpected discovery that specific low-copy number retrotransposons are mobile in the pollen of some maize lines, but not of others. We conducted large-scale genetic experiments to isolate new bz mutations from several Bz stocks and recovered spontaneous stable mutations only in the pollen parent in reciprocal crosses. Most of the new stable bz mutations resulted from either insertions of low-copy number long terminal repeat (LTR) retrotransposons or deletions, the same two classes of mutations that predominated in a collection of spontaneous wx mutations [Wessler S (1997) The Mutants of Maize, pp 385–386]. Similar mutations were recovered at the closely linked sh locus. These events occurred with a frequency of 2–4 × 10−5 in two lines derived from W22 and in 4Co63, but not at all in B73 or Mo17, two inbreds widely represented in Corn Belt hybrids. Surprisingly, the mutagenic LTR retrotransposons differed in the active lines, suggesting differences in the autonomous element make-up of the lines studied. Some active retrotransposons, like Hopscotch, Magellan, and Bs2, a Bs1 variant, were described previously; others, like Foto and Focou in 4Co63, were not. By high-throughput sequencing of retrotransposon junctions, we established that retrotranposition of Hopscotch, Magellan, and Bs2 occurs genome-wide in the pollen of active lines, but not in the female germline or in somatic tissues. We discuss here the implications of these results, which shed light on the source, frequency, and nature of spontaneous mutations in maize.",
keywords = "Inbred variation, LTR retrotransposon, Maize, Male sporogenesis, Spontaneous mutation",
author = "Dooner, {Hugo K.} and Qinghua Wang and Huang, {Jun T.} and Yubin Li and Limei He and Wenwei Xiong and Chunguang Du",
year = "2019",
month = "5",
day = "28",
doi = "10.1073/pnas.1903809116",
language = "English",
volume = "166",
pages = "10734--10743",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "22",

}

Spontaneous mutations in maize pollen are frequent in some lines and arise mainly from retrotranspositions and deletions. / Dooner, Hugo K.; Wang, Qinghua; Huang, Jun T.; Li, Yubin; He, Limei; Xiong, Wenwei; Du, Chunguang.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 166, No. 22, 28.05.2019, p. 10734-10743.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Spontaneous mutations in maize pollen are frequent in some lines and arise mainly from retrotranspositions and deletions

AU - Dooner, Hugo K.

AU - Wang, Qinghua

AU - Huang, Jun T.

AU - Li, Yubin

AU - He, Limei

AU - Xiong, Wenwei

AU - Du, Chunguang

PY - 2019/5/28

Y1 - 2019/5/28

N2 - While studying spontaneous mutations at the maize bronze (bz) locus, we made the unexpected discovery that specific low-copy number retrotransposons are mobile in the pollen of some maize lines, but not of others. We conducted large-scale genetic experiments to isolate new bz mutations from several Bz stocks and recovered spontaneous stable mutations only in the pollen parent in reciprocal crosses. Most of the new stable bz mutations resulted from either insertions of low-copy number long terminal repeat (LTR) retrotransposons or deletions, the same two classes of mutations that predominated in a collection of spontaneous wx mutations [Wessler S (1997) The Mutants of Maize, pp 385–386]. Similar mutations were recovered at the closely linked sh locus. These events occurred with a frequency of 2–4 × 10−5 in two lines derived from W22 and in 4Co63, but not at all in B73 or Mo17, two inbreds widely represented in Corn Belt hybrids. Surprisingly, the mutagenic LTR retrotransposons differed in the active lines, suggesting differences in the autonomous element make-up of the lines studied. Some active retrotransposons, like Hopscotch, Magellan, and Bs2, a Bs1 variant, were described previously; others, like Foto and Focou in 4Co63, were not. By high-throughput sequencing of retrotransposon junctions, we established that retrotranposition of Hopscotch, Magellan, and Bs2 occurs genome-wide in the pollen of active lines, but not in the female germline or in somatic tissues. We discuss here the implications of these results, which shed light on the source, frequency, and nature of spontaneous mutations in maize.

AB - While studying spontaneous mutations at the maize bronze (bz) locus, we made the unexpected discovery that specific low-copy number retrotransposons are mobile in the pollen of some maize lines, but not of others. We conducted large-scale genetic experiments to isolate new bz mutations from several Bz stocks and recovered spontaneous stable mutations only in the pollen parent in reciprocal crosses. Most of the new stable bz mutations resulted from either insertions of low-copy number long terminal repeat (LTR) retrotransposons or deletions, the same two classes of mutations that predominated in a collection of spontaneous wx mutations [Wessler S (1997) The Mutants of Maize, pp 385–386]. Similar mutations were recovered at the closely linked sh locus. These events occurred with a frequency of 2–4 × 10−5 in two lines derived from W22 and in 4Co63, but not at all in B73 or Mo17, two inbreds widely represented in Corn Belt hybrids. Surprisingly, the mutagenic LTR retrotransposons differed in the active lines, suggesting differences in the autonomous element make-up of the lines studied. Some active retrotransposons, like Hopscotch, Magellan, and Bs2, a Bs1 variant, were described previously; others, like Foto and Focou in 4Co63, were not. By high-throughput sequencing of retrotransposon junctions, we established that retrotranposition of Hopscotch, Magellan, and Bs2 occurs genome-wide in the pollen of active lines, but not in the female germline or in somatic tissues. We discuss here the implications of these results, which shed light on the source, frequency, and nature of spontaneous mutations in maize.

KW - Inbred variation

KW - LTR retrotransposon

KW - Maize

KW - Male sporogenesis

KW - Spontaneous mutation

UR - http://www.scopus.com/inward/record.url?scp=85066244697&partnerID=8YFLogxK

U2 - 10.1073/pnas.1903809116

DO - 10.1073/pnas.1903809116

M3 - Article

C2 - 30992374

AN - SCOPUS:85066244697

VL - 166

SP - 10734

EP - 10743

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 22

ER -